Corresponding author: Brian M. Connolly ( firstname.lastname@example.org )
Academic editor: Tiffany Knight
© 2017 Brian M. Connolly, Jennifer Powers, Richard N. Mack.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Connolly BM, Powers J, Mack RN (2017) Biotic constraints on the establishment and performance of native, naturalized, and invasive plants in Pacific Northwest (USA) steppe and forest. NeoBiota 34: 21-40. https://doi.org/10.3897/neobiota.34.10820
Factors that cause differential establishment among naturalized, invasive, and native species are inadequately documented, much less often quantified among different communities. We evaluated the effects of seed addition and disturbance (i.e., understory canopy removal) on the establishment and seedling biomass among two naturalized, two invasive, and two native species (1 forb, 1 grass in each group) within steppe and low elevation forest communities in eastern Washington, USA. Establishment within each plant immigrant class was enhanced by seed addition: naturalized species showed the greatest difference in establishment between seed addition and no seed addition plots, native and invasive species establishment also increased following seed addition but not to the same magnitude as naturalized species. Within seed addition plots, understory canopy disturbance resulted in significant increases in plant establishment (regardless of plant immigration class) relative to undisturbed plots and the magnitude of this effect was comparable between steppe and adjacent forest. However, regardless of disturbance treatment fewer invasive plants established in the forest than in the steppe, whereas native and naturalized plant establishment did not differ between the habitats. Individual biomass of naturalized species were consistently greater in disturbed (canopy removed) versus undisturbed control plots and naturalized species were also larger in the steppe than in the forest at the time of harvest. Similar trends in plant size were observed for the native and invasive species, but the differences in biomass for these two immigration classes between disturbance treatments and between habitats were not significant. We found that strong limitations of non-native species is correlated with intact canopy cover within the forest understory, likely driven by the direct or indirect consequences of low light transmittance through the arboreal and understory canopy. Considered collectively, our results demonstrate how seed limitation and intact plant ground cover can limit the abundance and performance of naturalized species in Pacific Northwest steppe and low elevation forest, suggesting that local disturbance in both habitats creates microsites for these species to establish and survive. Future studies evaluating interactions between multiple barriers to establishment using more representatives from each immigration class will further reveal how biotic interactions ultimately influence the demography and distribution of non-native plants within these communities.
Disturbance, seed limitation, biotic resistance, competition, mesic steppe, coniferous forest, seedling establishment, seedling performance
Naturalizations form the small fraction of those introduced species that have surmounted demographic and local environmental barriers to develop self-sustaining populations, but unlike invaders, naturalized species do not inevitably proliferate within the novel habitat (
The physical and biotic factors governing plant establishment are frequently quantified (e.g.,
The potential for a species’ immigrants to naturalize and the descendants to invade can also vary by habitat (
Meadow steppe and adjacent coniferous forest in eastern Washington (USA) have experienced markedly different levels of plant invasion. Non-native grasses and forbs are prevalent in steppe (
We examined the effect of seed addition and local disturbance (i.e., removal of all plant material <1.5 m above the ground) on the establishment and performance of native, naturalized, and invasive species in meadow-steppe and forest habitats in eastern Washington (USA) as part of a multi-pronged investigation of the forces that restrict/enhance naturalization (
A total of eight steppe and forest study sites were chosen that span the meadow steppe-xerophytic forest ecotone in eastern Washington (See Suppl. material
A seed mixture of three grasses and three forbs (a native, naturalized, and invasive species of each taxonomic category) was used in seed addition plots in this study. The native perennials Pseudoroegneria spicata and Geum triflorum are prevalent in meadow-steppe (
We substantiate the immigrant class (naturalized vs. invasive) of each non-native test species based on 1) a preliminary vegetation analysis conducted at all 8 study sites (
The effects of seed addition and disturbance were assessed in late July-early August 2011 in six experimental blocks arranged in a 2 × 3 grid at each site (25 × 50 m); blocks were 25-m apart. Each block was comprised of four hardware cloth exclosures (aboveground dimensions were 45 × 45 × 45 cm tall, 1 cm2 openings); exclosures in each experimental block were arranged 2-m apart in a square (24 exclosures per site, 192 exclosures total across all sites). Before its installation each exclosure was sprayed with enamel paint (Krylon®) to prevent leachate from the hardware cloth affecting plant growth within the exclosure. Exclosures were embedded 15-cm deep into the mineral soil to exclude the treatment being confounded by vertebrate seed predators.
Each block contained a complete 2 × 2 factorial cross with seed addition and disturbance as factors. To generate disturbance treatments, we removed all vegetation and litter from the soil surface and churned the top 3 cm of mineral soil without removing any soil. Disturbed soil was then leveled within each exclosure to minimize differences in soil microtopography among these exclosures (
In early August 2011, 96 exclosures amongst the sites were sown with an admixture of seeds containing three grasses (P. spicata, S. cereale, B. tectorum) and the three forbs (G. triflorum, Ce. cyanus, Ci. arvense). Seeds were sown evenly across a 30 × 30 cm square at the center of each exclosure (0.09 m2 sampling area, 50 seeds of each species, 300 seeds sown total per exclosure). Seeds were pressed firmly onto the soil surface to minimize post-dispersal seed movement. In the remaining 96 exclosures amongst the sites no seeds were added in order to measure natural recruitment of study species and evaluate the contribution of seed addition to plant establishment counts.
Exclosures were monitored monthly for damage and other extraneous events; plants were counted in early July 2012 to estimate establishment. Following July counts, all above ground plant biomass was harvested within each exclosure, separated by species, dried (48 hours at 70°C) and weighed. Plant establishment was quantified early in the growing season and before the production of reproductive structures in order to minimize the possibility of introducing non-native species. Natural recruitment by species other than our six test species was rare within these exclosures; nonetheless these recruits were excluded from the analysis. Average individual seedling biomass was estimated by dividing total biomass for each species in each exclosure by the number of that species in the exclosure. Plots that received seed addition were treated with glyphosate herbicide (Roundup®, Monsanto Company) at the cessation of the study. Additionally, the immediate area in a 15-m radius surrounding each exclosure was monitored throughout 2012 and 2013 to detect and remove extraneous introductions.
We used general linear mixed models to evaluate whether seed addition, disturbance, and plant immigration class (Native vs. Naturalized vs. Invasive) influenced the number of individuals that established within each community (Steppe vs. Forest). July individual counts of each species were averaged across all blocks at a site to generate site-level averages for each treatment combination and for each species. Ten exclosures were damaged in March 2011. These units were excluded from analysis as vertebrate seed predators and grazers can strongly influence plant establishment in these habitats (
Analysis of average individual biomass followed a similar model structure but was limited to seed addition plots to insure the analysis was conducted between individuals with similar durations of residence time within each plot. Individual biomass estimates of each species were averaged across all blocks at a site to generate site-level averages for each treatment combination and for each species. Individual biomasses were square-root transformed before analysis. Average Ci. arvense biomass at one steppe site (Smoot Hill - Summit) was a significant outlier differing from the species’ other mean values by over three standard errors and was driven by the rapid second year growth of an adult Ci. arvense already residing in the plot. Omitting this observation permits the analysis to satisfy assumptions of normality; consequently, final model analysis for average individual biomass did not include this observation. Models evaluating plant establishment and biomass employed the Kenward-Roger approximation to estimate appropriate degrees of freedom (
Our experimental design incorporated the effect of plant immigration class (Native, Naturalized, or Invasive) by evaluating two representative species from each class (one grass, one forb). Although the species selected represent common or dominant plants in these forest and steppe communities (See Study species section) and site-level quality can be assessed by the relative abundance of these native and non-native species (
Not surprisingly seed addition plots had greater recruitment than plots without seed addition, but the magnitude of the positive effects of seed addition varied by habitat and disturbance treatment (Table
General linear mixed model analysis describing the influence of habitat, disturbance, seed addition, plant introduction class, and all possible interactions of these fixed factors on the log-transformed individual counts of plots established in Pacific Northwest steppe and forest communities. Significant differences at a Type I Error = 0.05 are indicated in bold; marginally significant differences at Type I Error = 0.10 are indicated in italics.
|Factor||log (Plant Number + 1)|
|Habitat (H)||15.77||1, 6||0.007|
|Disturbance (D)||35.11||1, 18||<0.001|
|Seed Addition (SA)||598.78||1, 18||<0.001|
|H × D||19.93||1, 18||<0.001|
|H × SA||27.40||1, 18||<0.001|
|D × SA||98.89||1, 18||<0.001|
|H × D × SA||4.15||1, 18||0.057|
|Introduction Class (IC)||0.12||2, 144||0.885|
|IC × H||4.54||2, 144||0.012|
|IC × D||1.36||2, 144||0.261|
|IC × SA||9.62||2, 144||<0.001|
|IC × H × D||0.62||2, 144||0.542|
|IC × SA × H||1.47||2, 144||0.234|
|IC × SA × D||0.11||2, 144||0.892|
|IC × H × D × SA||0.03||2, 144||0.968|
Effect of habitat (Forest versus Steppe), disturbance (Disturbed [“Dist+”] versus Undisturbed [“Dist-”]), and seed addition (Seed Addition versus No Seed Addition) on the average number of total plants in each plot in July 2012. All plant counts are log(x+1) transformed and responses are reported as least square means estimates ± SE. Post hoc multiple pairwise comparisons were conducted with the Tukey-Kramer method; different lowercase letters indicate significant differences at a Type I error = 0.05.
Effect of habitat (A) [Forest versus Steppe] and seed addition (B) [Seed Addition versus No Seed Addition] on the average number of native (“NTV”), naturalized (“NTZ”), and invasive (“INV”) plants in each plot in July 2012. All plant counts are log(x+1) transformed and responses are reported as least square means estimates ± SE. Post hoc multiple pairwise comparisons were conducted with the Tukey-Kramer method; different lowercase letters indicate significant differences at a Type I error = 0.05.
Individual plant biomass was influenced by a significant interaction between plant immigration class and habitat and a marginally significantly interaction between plant immigration class and disturbance treatment (Table
General linear mixed model analysis describing the influence of habitat, disturbance, plant introduction class, and the interaction of these fixed factors on the square root-transformed individual biomass of plants harvested (July 2012) from plots established in Pacific Northwest steppe and forest communities. Significant differences at Type I Error = 0.05 indicated in bold; marginally significant differences at Type I Error = 0.10 are indicated in italics.
|Habitat (H)||13.96||1, 6.0||0.010|
|Disturbance (D)||125.17||1, 6.2||<0.001|
|Introduction Class (IC)||77.61||2, 72.2||<0.001|
|H × D||0.52||1, 6.2||0.498|
|IC × H||5.41||2, 72.2||0.007|
|IC × D||2.46||2, 72.2||0.093|
|IC × H × D||0.07||2, 72.2||0.931|
Effect of habitat (A) [Forest versus Steppe] and disturbance (B (Disturbed [“Dist+”] versus Undisturbed [“Dist-”]) on the average individual biomass of native (“NTV”), naturalized (“NTZ”), and invasive (“INV”) plants in each plot as of July 2012. Individual plant biomass estimates were square root-transformed prior to analysis and responses are reported as least square means estimates ± SE. Values are derived solely from seed addition (SA+) plots to insure comparisons were conducted between individuals with similar durations of residence time within each plot. Post hoc multiple pairwise comparisons were conducted with the Tukey-Kramer method; different lowercase letters indicate significant differences at a Type I error = 0.05.
Our goal was to determine whether seed limitation and disturbance via canopy removal differentially influence the recruitment and performance of native, naturalized, and invasive species in communities (meadow steppe and coniferous forest) that differ radically in physiognomy. Seed limitation differed among the three class with naturalized species the most seed limited, native species intermediately limited, and invaders experiencing intermediate to no limitation. We found that intact plant cover restricts seedling establishment similarly across all plant immigrant class and also results in significantly lower naturalized species growth. Low abundance among naturalized species in PNW meadow steppe and low recruitment of most non-native species in the forest understory are at least partially attributable to the combined influence of seed limitation and low resource availability mitigated by understory canopy cover (e.g., light levels at the soil surface, Suppl. material
Seed limitation influences recruitment of many native (
Differences in species’ biomass production between habitat types and with or without disturbance may also influence non-native propagule pressure and contribute to seed limitation for non-native species. For example, individual B. tectorum biomass correlates strongly with total seed mass produced per individual plant (R2adj = 0.861; P < 0.001,
Disturbance can facilitate a species’ transition from naturalization to invasion (
Competition in the PNW coniferous forest understory is a strong biotic barrier to invasive species that are abundant in the adjacent steppe, particularly B. tectorum (
The environmental tolerances of introduced species interact with a novel habitat to determine a species’ potential for naturalization (
Few studies directly evaluate the relationship between biotic resistance and the relative abundance of introduced species (
We thank two anonymous reviewers and T. Knight for constructive feedback on the submitted versions of this manuscript. We thank M. Dybdahl, D. Pearson, and L. Carris for helpful comments on earlier drafts of this manuscript. We thank D. Savage and the WSU technical services instrument shop for assistance with exclosure construction. We thank M. Rule for assistance with site identification and permit preparation at the Turnbull National Wildlife Refuge. The Betty Higginbotham trust at Washington State University provided funding to support this work, and AFRI-NIFA Fellowship grant #2014-02074 awarded to B. Connolly provided support while writing this manuscript.